electromechanical delay of the knee flexor muscles after
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University of Nebraska at Omaha University of Nebraska at Omaha
DigitalCommons@UNO DigitalCommons@UNO
Journal Articles Department of Biomechanics
2011
Electromechanical Delay of the Knee Flexor Muscles After Electromechanical Delay of the Knee Flexor Muscles After
Harvesting the Hamstrings for Anterior Cruciate Ligament Harvesting the Hamstrings for Anterior Cruciate Ligament
Reconstruction Reconstruction
Stavros Ristanis University of Ioannina
Elias Tsepis Technological Educational Institution of Patras at Aigion
Dimitrios Giotis University of Ioannina
Franceska Zampeli University of Ioannina
Nikolaos Stergiou University of Nebraska at Omaha, [email protected]
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Recommended Citation Recommended Citation Ristanis, Stavros; Tsepis, Elias; Giotis, Dimitrios; Zampeli, Franceska; Stergiou, Nikolaos; and Georgoulis, Anastasios D., "Electromechanical Delay of the Knee Flexor Muscles After Harvesting the Hamstrings for Anterior Cruciate Ligament Reconstruction" (2011). Journal Articles. 144. https://digitalcommons.unomaha.edu/biomechanicsarticles/144
This Article is brought to you for free and open access by the Department of Biomechanics at DigitalCommons@UNO. It has been accepted for inclusion in Journal Articles by an authorized administrator of DigitalCommons@UNO. For more information, please contact [email protected].
Authors Authors Stavros Ristanis, Elias Tsepis, Dimitrios Giotis, Franceska Zampeli, Nikolaos Stergiou, and Anastasios D. Georgoulis
This article is available at DigitalCommons@UNO: https://digitalcommons.unomaha.edu/biomechanicsarticles/144
Electromechanical Delay of the Knee Flexor Muscles After Harvesting
the Hamstrings for Anterior Cruciate Ligament Reconstruction
Stavros Ristanis, MD,* Elias Tsepis, PT, PhD,† Dimitrios Giotis, MD,* Franceska Zampeli,
MD,* Nicholas Stergiou, PhD,‡§ and Anastasios D. Georgoulis, MD*
From the *Orthopaedic Sports Medicine Center of Ioannina, Department of Orthopaedic Surgery,
University of Ioannina, Ioannina, Greece; †Physical Therapy Department, Technological Educational
Institution of Patras, Aigion, Greece; ‡Nebraska Biomechanics Core Facility, University of Nebraska at
Omaha, Omaha, Nebraska; and §Department of Environmental, Agricultural, and Occupational Health,
College of Public Health, University of Nebraska Medical Center, Omaha, Nebraska.
Objective: To investigate if harvesting of semitendinosus (ST) and gracilis for anterior cruciate ligament
(ACL) reconstruction will have an effect in coordinative firing pattern of the hamstrings under fatigue.
We hypothesized that fatigue will increase the electromechanical delay (EMD) of the hamstrings on the
harvested site and impair the synchronization between the medial and lateral hamstrings, in terms of
muscle activity onsets.
Design: Prospective nonrandomized study. Setting: Institutional. Patients: Twelve ACL reconstructed
patients with hamstrings, 2 years postoperatively.
Interventions: The patients performed a fatigue protocol with 25 continuous maximal isometric
voluntary contractions of 8-second duration with 2-second intervals. Main Outcome Measures: The
electromyography activity of biceps femoris (BF) and ST was recorded bilaterally and simultaneously
with the torque measurements. The dependent variable examined was the EMD difference between BF
and ST (muscle activation pattern).
Results: The fatigue protocol caused significant differences for the EMD values for both the intact and
the reconstructed leg, demonstrating the influence of fatigue in EMD. However, the synchronization
pattern between the medial and lateral hamstrings did not change significantly throughout the fatiguing
protocol, revealing a balanced effect of fatigue.
Conclusions: Although the EMD of ST and BF was significantly increased due to fatigue, as expected,
their synchronization pattern as identified by the difference in their EMDs remained the same. Thus, the
reconstructed knee responded in a balanced manner and the hamstrings firing pattern remained the
same, despite the intervention to the ST tendon.
Key Words: electromechanical delay, ACL reconstruction, hamstrings, electromyography, fatigue,
muscle synchronization
Introduction
The use of hamstrings for anterior cruciate ligament (ACL) reconstruction has increased in recent years.
Biomechanical studies have demonstrated that this graft exhibits comparable strength and stiffness to
the native ACL.1,2 However, many surgeons are still skeptical about postoperative functionality because
some research has demonstrated impaired recovery in extended follow-ups.3 The majority of studies
have focused on evaluating strength of the hamstrings, after harvesting of their tendons.4 However,
some investigators have suggested that the actual effectiveness of the muscles to provide appropriate
mechanical response and protection under real-life situations can be revealed only with the
measurement of the time delay between the onset of muscle stimulation by the alpha motoneuron and
the development of the corresponding torque at the joint.5–7 This is referred to as the electromechanical
delay (EMD).5 The measurement of the EMD is of great functional importance because regardless of the
contractile ability of the muscles, alterations in the EMD of the hamstrings muscle-tendon unit could
compromise knee integrity or impair performance by modifying the transfer time of muscle tension to
the bones.5–7
Factors related to the EMD include the mechanical properties of the in-series elastic components of the
muscle, the size and length of the muscle, as well as its fiber type composition, and the presence of
fatigue.8–11 Muscle fatigue, which has been defined as any reduction in the force-generating capacity of
the entire neuromuscular system regardless of the force expected, 12 is common in sports activities.
Fatigue can affect not only the force-generating capacities but also the temporal characteristics of the
neuromuscular mechanism, and especially the EMD.10 Therefore, changes in the EMD should be
expected under muscle fatigue conditions.
In the present study, we tried to identify how fatigue impairs the knee flexor mechanism in terms of the
EMD, after harvesting the semitendinosus (ST) and gracilis (G) muscle tendons for ACL reconstruction.
Our methodology (surface electromyography) allowed us to evaluate only the ST muscle and not the G
muscle. In addition, we decided to investigate the biceps femoris (BF) to ensure a more comprehensive
evaluation of the hamstrings. Although BF is not anatomically involved in the operation, investigation of
its EMD could be useful because synchronization between the medial and lateral hamstrings is
important for knee rotational stability.13 Our rationale for this inclusion was that if changes exist in the
EMD of the ST, then changes in the BF may also appear, due to the fact that these 2 muscles act as a
coordinated unit when the knee flexor mechanism is initiated.14 If not, then this could generate a major
synchronization issue on the hamstrings muscle response firing pattern.
Therefore, the purpose of this study was to investigate whether muscle fatigue actually affected the
EMD of the hamstrings 2 years after ACL reconstruction and if the coordination between the medial and
the lateral hamstrings was disturbed. We hypothesized that fatigue of the knee flexors after harvesting
of the ST/G tendons for ACL surgery will (1) increase the EMD of the hamstrings on the harvested site
and (2) impair the synchronization between the medial and lateral hamstrings, in terms of muscle
activation as evaluated with the EMD.
Methods
Subjects
We examined 12 ACL reconstructed patients with a quadrupled hamstrings (ST/G) graft (men: mean age,
26 ± 8 years; mean mass, 74 ±14 kg; mean height, 1.72 ± 0.10 m), approximately 2 years (range, 24-26
months) after the operation. They all followed the same postoperative rehabilitation program. Return to
sports-related activities was permitted 24 weeks after reconstruction, provided that the patients had
regained full strength and stability. Their strength at that time was determined with the BIODEX
(System-3; Biodex, Corp, Shirley, New York) isokinetic dynamometer, revealing acceptable symmetry in
quadriceps and hamstrings strength, as well as satisfactory agonist to antagonist ratios. At the time of
data collection, no clinical evidence of knee pain was found.
Surgical Reconstruction With a Quadrupled ST/G Graft
Through a 4 to 5 cm longitudinal skin incision over the pes anserinus, a typical harvesting of both the ST
and the G tendons was performed in all patients. The tibial tunnel was prepared with the knee in 90°
flexion. The hole in the tibial plateau was placed approximately 5 mm anterior and medial to the
anatomic center of the natural ACL attachment.15 Subsequently, the femoral tunnel was drilled with the
knee flexed in 120°, through the anteromedial portal at the 10-o’clock position (for a right knee). The
graft was secured at the distal femur with an EndoButton (Smith & Nephew Endoscopy, Andover,
Massachusetts) and fixated at the tibial tunnel with a bioabsorbable screw.
Clinical Evaluation
Before any data collection, a clinical evaluation was performed for all subjects. During this evaluation,
the Lysholm functional score, the Tegner activity scale, and the International Knee Documentation Score
(IKDC) Subjective Knee Evaluation Form were also obtained.16 Anterior tibial translation was evaluated
using the KT-1000 knee arthrometer (MEDmetric Corp, San Diego, California) for both limbs of the ACL
reconstructed group.17 The measurements were performed using 134N posterior-anterior external force
at the tibia, and maximum posterior-anterior external force until heel clearance. Repeated anterior
tractions were performed until a constant reading on the dial was registered.
EMD Measurement
The method used to measure the EMD has been described in detail elsewhere.18, 19 Briefly, the patients
sat on the testing chair of the dynamometer, with the knee and hip joint flexed at 30°. Torque
measurements were performed for both knees using the Biodex isokinetic dynamometer. All the
subjects were instructed to exert a maximum knee flexion as fast and as hard as possible, after hearing a
specific sound generated by the dynamometer. The subject held the maximal force, until the sound
stopped. Each subject performed 1-leg fatiguing exercise, which consisted of 25 such maximally
explosive isometric voluntary contractions. Each contraction lasted 8 seconds and was followed by 2-
second relaxation between each contraction, according to the fatigue protocol developed from Zhou.20
Electromyography (EMG) traces were recorded from both the ACL reconstructed and the intact
contralateral leg simultaneously with the torque measurements, with a wireless 8-channel EMG system
(Telemyo 2400T; Noraxon, Scottsdale, Arizona), and were displayed real time on a computer using
dedicated software (MyoResearchXP; Noraxon). Surface electromyography was obtained from the ST
and BF muscles bilaterally using bipolar, circular, preamplified, Ag/AgCl electrodes with 10 mm diameter
and fixed interelectrode spacing of 20mm(Noraxon). The electrodes were attached parallel to the
muscle fibers and over the dorsomedial muscle bulge at two-thirds of the proximodistal thigh length for
the ST and at the dorsolateral side of the thigh at half of the proximodistal thigh length for the BF. The
subjects were instructed to relax the muscles completely before a contraction trial.
Before the test, all subjects were instructed to stay completely relaxed in the Biodex testing chair, while
the EMG signal was calibrated with the ‘‘zero offset’’ function to establish a zero baseline from each of
the EMG channels. The EMG signals were acquired at a sampling rate of 1000 Hz. The root-mean-square
(RMS) amplitude for each muscle burst was calculated as follows: the raw EMG signals were measured
in a band of 10 to 500 Hz, full-wave rectified, high-pass filtered with a Butterworth filter to remove
movement artifacts with a cutoff frequency of 20 Hz, and smoothed with a 100-millisecond RMS
algorithm. Measurements of the EMD were performed using the isokinetic dynamometer and the
surface EMG unit, according to the protocol developed by Zhou et al.11 Based on this protocol, the
onset of torque development is defined as a 3.6-Nm deviation above the baseline level and 615 mV
deviation from the baseline for the EMG signal.
Statistical Analysis
To address the hypothesis that fatigue of the knee flexors after harvesting of the ST/G tendons for ACL
surgery will increase the EMD of the hamstrings on the harvested site, we performed paired t tests on
the actual values of the EMD of BF and the EMD of ST for each leg between the first 5 and the last 5
trials of the fatigue protocol. To address the second hypothesis that fatigue of the knee flexors after
harvesting of the ST/G tendons for ACL surgery will impair the synchronization between the medial and
lateral hamstrings, we examined the coordination of the hamstrings in terms of muscle activation onsets
by subjecting the difference in the EMDs between the BF and ST (Figure 1) in a 2-way fully repeated
analysis of variance (ANOVA).
The ANOVA factors were identified as Leg (Intact Contralateral vs ACL Reconstructed) and Fatigue (Trial
1 vs. vs Trial 25). Practically, the factor Leg had 2 levels and the factor Fatigue had 25 levels. Tukey post
hoc comparisons were used to locate differences when significance was identified. An additional post
hoc evaluation was performed to verify the ANOVA outcomes and to explore if grouping the trials would
affect these results. Thus, we also performed paired t tests on the same dependent variable (the
difference in the EMDs between the BF and ST) between the first 5 trials and the last 5 trials for both the
intact and the ACL reconstructed leg and for both investigated muscles. The statistical significance was
set at 0.05. All the statistical comparisons were performed with the Statistica (v.8 software; StatSoft, Inc,
Tulsa, Oklahoma).
Ethical Considerations
All subjects agreed with the testing protocol and gave their consent to participate in accordance with
the Institutional Review Board policies of the University of Ioannina Medical School.
Results
Negative Lachman and pivot-shift tests indicated that the knee joint stability was regained clinically for
all ACL reconstructed subjects. The median Lysholm score was 92 (range, 87-95), the Tegner score was 7
(range, 6-8), and the IKDC score was scaled as normal (A) at the time of examination. KT-1000 results
revealed that the mean difference between the anterior tibial translation of the reconstructed and
intact sides in the ACL reconstructed group was 1.1 mm (range, 0.5-2 mm) for the 134N test and 1.3 mm
(range, 1-2 mm) for the maximum manual test, respectively. No significant differences were found for
the KT-1000 results between the limbs.
With respect to our first hypothesis, the t test comparisons between the first 5 and the last 5 trials of
the fatigue protocol showed significant increases for the actual EMD values for both the intact (P = 0.002
for BF and P = 0.008 for ST) and the reconstructed leg (P = 0.023 for BF and P = 0.025 for ST), revealing
the effect of fatigue on EMD clearly (Figure 2). However, when we evaluated the EMD difference
between the BF and ST, we found no significant interaction for the coordination of the hamstrings
muscle firing pattern for both legs (F = 0.67; P = 0.878) (Figure 3). We also found no significant
differences for the Leg factor (F = 1.027; P = 0.335) and the Fatigue factor (F = 1.061; P = 0.390). In
addition, the paired t test comparison for the same parameter (the EMD difference between the BF and
ST) between the first 5 and the last 5 trials of the fatigue protocol showed no significant differences for
both the intact and the ACL reconstructed leg (P = 0.108 and P = 0.398, respectively), verifying our
ANOVA results and indicating that fatigue does not affect this coordination pattern.
Discussion
Based on the results from our previous work,18 we hypothesized in the present study that fatigue of the
knee flexors after harvesting of the ST/G tendons for ACL surgery will (1) increase the EMD of the
hamstrings on the harvested site and (2) impair their coordination, in terms of muscle activation, as
evaluated with EMD. Our results supported our first hypothesis and refuted our second. Specifically, we
found that although fatigue affected both medial and lateral hamstrings EMD, their coordinated firing
pattern remained the same for the 2 legs throughout the fatiguing protocol. This finding is of great
importance because it demonstrates that although we had harvested the ST tendon (resulting in
postoperative alterations in the muscle’s size, length, and fiber type composition), the coordinative
firing pattern of the investigated muscles remained the same, continuing to synchronize in the same
way as the intact, thus achieving balance between and within legs.
In our protocol, fatigue was induced in the form of repetitive isometric contractions, which is a protocol
that is well established in the literature.8, 11 Fatigue depresses force generation capacity during either
static or dynamic muscle contractions.21 Despite the possible effects of central fatigue, the decreased
muscle contractile performance during fatigue has been related to impairment of membrane
excitability, reduction in titanic cytosolic calcium (Ca+2) concentration, reduced myofibril Ca+2 sensitivity,
and the direct inhibitory effects of phosphate and hydrogen ions on force generation.21,22 Because EMD
measures the time lapse from muscle activation until a certain threshold of muscle tension is developed,
muscle fatigue, which affects the aforementioned processes, is expected to prolong the EMD.
However, despite the numerous investigations in the area of muscle fatigue, its effect on EMD remains
controversial. There have been reports that the EMD increased after fatiguing dynamic exercise,23
whereas other studies have showed no significant change in EMD after repeated dynamic or isometric
contractions.7 Kroll24 had shown no significant changes of EMD after a fatigue protocol that involved
bench stepping exercise and a plantar flexor fatigue. Vos et al7 also found no significant change in EMD
of the rectus femoris muscle after 150 repetitions of 50% isometric maximal voluntary contraction. On
the other hand, Nilsson et al25 have shown a significant lengthening of EMD after a fatigue protocol.
Similarly, Zhou20 studied the effects of fatigue on the EMD of the knee extensor muscles and showed a
significant increase in EMD after a fatigue protocol that included 4 periods of 30 seconds of an all-out
sprint cycling exercise. Horita and Ishiko23 also reported that the EMD was affected by repeated maximal
isokinetic knee extensions. In our study, we also found significantly increased EMD values for BF and ST
muscles at the end of the fatigue protocol. The discrepancies between the above studies are probably
related to the different types of muscle contractions used and the variability in the fatigue protocols.
Our methodology allowed us to evaluate only the ST muscle and not the G muscle. In addition, we
decided to investigate the BF to ensure a more comprehensive evaluation of the hamstrings. Rotatory
stability of the knee is a major concern for knee protection and because it is impaired after ACL injury, in
the current study, we focused on investigating if the EMD of the BF shows a different pattern than the
EMD of the lateral hamstrings. A possible difference would question knee stability under fatigue, after
using the hamstrings tendons as a graft. Our results showed that the BF-ST firing pattern remained the
same for both legs of the ACL reconstructed individuals throughout the fatigue protocol, even though
the EMD values for each muscle separately were affected by the fatigue protocol, as expected. A
possible explanation for the lack of changes of the BF-ST firing pattern is that the BF works
synergistically with the ST during knee flexion to provide functional balance to the knee. Changes in the
EMD of the ST may also be accompanied by changes in the BF, due to the fact that these 2 muscles act
as a unit when the knee flexor mechanism is initiated.14,26
Several studies have emphasized the importance of muscular alterations after injury to achieve joint
stability.14,26 Johansson et al26 suggested that joint stability is achieved by the continuous adjustment of
muscle activity around the joint (cocontraction). The ACL is loaded and potentially injured via anterior
tibial translation.27 The hamstrings are synergistic to the ACL, providing posterior tibial shear force,
which limits ACL loading attributable to anterior tibial translation.28 Noncontact ACL injury typically
occurs during landing and gait activities,29 which incur rapid changes in the forces applied to the knee
joint. As such, timely dynamic response from the hamstrings seems to be essential for ensuring knee
joint stability and limiting the load imparted to the ACL or its substitute graft in reconstructed patients.
A change in the hamstrings muscle activation pattern could actually prove detrimental for knee joint
stability and protection of the graft. This is why the evaluation of the EMD measurement is of great
functional importance. Regardless of the contractile ability of the muscles, which is depicted usually by
measuring knee flexion peak torque, alterations in the EMD of the donor-site muscle-tendon unit could
compromise knee integrity or impair performance by modifying the transfer time of muscle tension to
the bones.
Limitations in this study include the absence of a specific methodology in the literature for determining
EMD and defining specific threshold levels of both signals, onset of EMG, and force generation.
Reported values for EMD differ substantially across muscles and investigations due to differences in
operational definitions,30 characteristics of the muscles being tested,31 contraction type,6,11 and data
processing techniques.32 Corcos et al32 evaluated biceps brachii EMD under various experimental
conditions, including differences in hardware sensitivity, characteristics of the subject-force sensor
interface, and time-scale resolution, and reported significantly different EMD values as functions of the
various experimental characteristics. Another limitation of our study is the use of surface electrodes to
acquire the EMD measurements. However, similar procedures have been used in previous studies and
are considered reliable.7,23,33
In conclusion, we found that although the EMD of ST and BF was significantly increased due to fatigue
protocol as expected, their synchronization pattern remained the same, as the reconstructed knee
responded in a balanced manner. The hamstrings coordinative firing pattern remained the same,
despite the intervention to the ST tendon. Therefore, harvesting the ST/G tendon for ACL reconstruction
seems to have no effect on the coordinative firing pattern of knee flexors. This may be an important
preventive mechanism for the anterior cruciate ligament reconstructed athlete because possible
modifications in hamstrings response under fatigue conditions could have endangered knee balance and
increased the potential for reinjury.
Acknowledgements
The authors gratefully acknowledge the funding support from the Greek State Scholarships Foundation
in the form of a postdoctoral fellowship awarded to Dr. Stavros Ristanis.
Figure 1. A typical time plot of a single trial on the presentation of the stimulus (sound signal) to the
onset of the EMG signal for both muscles (ST and BF) and force generation (torque). The onset of torque
development is defined as a 3.6 Nm deviation above the baseline level and the onset of EMG signal as
±15 µV deviation above the baseline. The EMD difference (muscle sequence firing pattern) is indicated
with small arrow (EMD of BF 2 EMD of ST).
Figure 2. A line graph indicating the influence of fatigue in EMD values of a separate muscle (ST) of the
intact leg in a randomly selected patient from the examined group. The black line represents the 12 first
trials, whereas the gray line represents the last 12 trials of the fatigue protocol.
Figure 3. A line graph indicating the hamstrings muscle firing pattern for the intact (gray line) and the reconstructed leg (black line) in a randomly selected patient from the examined group. Although the EMDof ST and BF significantly increased during the fatigue protocol, we found that their coordination firing pattern remained the same during the fatigue protocol.
References 1. Chen L, Cooley V, Rosenberg T. ACL reconstruction with hamstring tendon. Orthop Clin North Am.
2003;34:9–18. 2. Hamner DL, Brown CH, Steiner ME, et al. Hamstring tendon grafts for reconstruction of the ACL:
biomechanical evaluation of the use of multiple strands and tensioning techniques. J Bone Joint Surg Am. 1999; 81:549–557.
3. Elmlinger BS, Nyland JA, Tillett ED. Knee flexor function 2 years after anterior cruciate ligament reconstruction with semitendinosus-gracilis autografts. Arthroscopy. 2006;22:650–655.
4. Lipscomb AB, Johnston RK, Snyder RB, et al. Evaluation of hamstring strength following use of semitendinosus and gracilis tendons to reconstruct the ACL. Am J Sports Med. 1982;10:340–342.
5. Cavanagh PR, Komi PV. Electromechanical delay in human skeletal muscle under concentric and eccentric contractions. Eur J Appl Physiol Occup Physiol. 1979;42:159–163.
6. Norman RW, Komi PV. Electromechanical delay in skeletal muscle under normal movement conditions. Acta Physiol Scand. 1979;106:241–248.
7. Vos EJ, Harlaar J, van Ingen Schenau GJ. Electromechanical delay during knee extensor contractions. Med Sci Sports Exerc. 1991;23:1187–1193.
8. Gabriel DA, Boucher JP. Effects of repetitive dynamic contractions upon electromechanical delay. Eur J Appl Physiol Occup Physiol. 1998;79: 37–40.
9. Zhou S, McKenna MJ, Lawson DL, et al. Effects of fatigue and sprint training on electromechanical delay of knee extensor muscles. Eur J Appl Physiol Occup Physiol. 1996;72:410–416.
10. Zhou S, Carey MF, Snow RJ, et al. Effects of muscle fatigue and temperature on electromechanical delay. Electromyogr Clin Neurophysiol. 1998;38:67–73.
11. Zhou S, Lawson DL, Morrison WE, et al. Electromechanical delay in isometric muscle contractions evoked by voluntary, reflex and electrical stimulation. Eur J Appl Physiol Occup Physiol. 1995;70:138–145.
12. Bigland-Ritchie B, Woods JJ. Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve. 1984;7:691–699.
13. Aagaard P, Simonsen EB, Andersen JL, et al. Antagonist muscle coactivation during isokinetic knee extension. Scand J Med Sci Sports. 2000;10:58–67.
14. Baratta R, Solomonow M, Zhou BH, et al. Muscular coactivation. The role of the antagonist musculature in maintaining knee stability. Am J Sports Med. 1988;16:113–122.
15. Clancy WG Jr, Nelson DA, Reider B, et al. Anterior cruciate ligament reconstruction using one-third of the patellar ligament, augmented by extra-articular tendon transfers. J Bone Joint Surg Am. 1982;64:352–359.
16. Tegner Y, Lysholm J. Rating systems in the evaluation of knee ligament injuries. Clin Orthop. 1985;198:43–49.
17. Steiner M, Brown C, Zarins B, et al. Measurement of anterior-posterior displacement of the knee. A comparison of the results with instrumented devices and with clinical examination. J Bone Joint Surg Am. 1990;72: 1307–1315.
18. Ristanis S, Tsepis E, Giotis D, et al. Electromechanical delay of the knee flexor muscles is impaired after harvesting hamstring tendons for anterior cruciate ligament reconstruction. Am J Sports Med. 2009;37:2179–2186.
19. Georgoulis AD, Ristanis S, Papadonikolakis A, et al. EMD of the knee extensor muscles is not altered after harvesting the patellar tendon as a graft for ACL reconstruction: implications for sports performance. Knee Surg Sports Traumatol Arthrosc. 2005;13:437–443.
20. Zhou S. Acute effect of repeated maximal isometric contraction on EMD of knee extensor muscle. J Electromyogr Kinesiol. 1996;6:117–127.
21. Maclaren DP, Gibson H, Parry-Billings M, et al. A review of metabolic and physiological factors in fatigue. Exerc Sport Sci Rev. 1989;17:29–66.
22. Westerblad H, Lee JA, La¨nnergren J, et al. Cellular mechanisms of fatigue in skeletal muscle. Am J Physiol. 1991;261:195–209.
23. Horita T, Ishiko T. Relationships between muscle lactate accumulation and surface EMG activities during isokinetic contractions in man. Eur J Appl Physiol Occup Physiol. 1987;56:18–23.
24. Kroll W. Fractionated reaction and reflex time before and after fatiguing isotonic exercise. Med Sci Sports. 1974;6:260–266.
25. Nilsson J, Tesch P, Thorstensson A. Fatigue and EMG of repeated fast voluntary contractions in man. Acta Physiol Scand. 1977;101:194–198.
26. Johansson H, Sjo¨lander P, Sojka P. Receptors in the knee joint ligaments and their role in the biomechanics of the joint. Crit Rev Biomed Eng. 1991;18:341–368.
27. DeMorat G, Weinhold P, Blackburn T, et al. Aggressive quadriceps loading can induce noncontact anterior cruciate ligament injury. Am J Sports Med. 2004;32:477–483.
28. MacWilliams BA, Wilson DR, DesJardins JD, et al. Hamstrings cocontraction reduces internal rotation, anterior translation, and anterior cruciate ligament load in weight-bearing flexion. J Orthop Res. 1999;17:817–822.
29. Griffin LY, Albohm MJ, Arendt EA, et al. Understanding and preventing noncontact anterior cruciate ligament injuries: a review of the Hunt Valley II meeting. Am J Sports Med. 2006;34:1512–1532.
30. Winter EM, Brookes FB. Electromechanical response times and muscle elasticity in men and women. Eur J Appl Physiol Occup Physiol. 1991;63:124–128.
31. Viitasalo J, Komi P. Interrelationships between electromyographic, mechanical, muscle structure and reflex time measurements in man. Acta Physiol Scand. 1981;111:97–103.
32. Corcos DM, Gottlieb GL, Latash ML, et al. Electromechanical delay: an experimental artifact. J Electromyogr Kinesiol. 1992;2:59–68.
33. Fauth ML, Petushek EJ, Feldmann CR, et al. Reliability of surface electromyography during maximal voluntary isometric contractions, jump landings and cutting. J Strength Cond Res. 2010;24:1131–1137.